Natural enemy ecology

Direct effects of predators on host-parasite interactions

This seems like quite an obvious point – being sick makes you easier to catch, so parasites should make infected individuals more vulnerable to predation. Surprisingly, this hypothesis has been little tested outside systems in which the parasite benefits from the predation event, but could have important implications for the evolution of both host and parasite. In the guppy-gyro system, we used startle responses as a proxy for vulnerability to predation, and found that while infection had a limited influence on large fish, small fish covered significantly less ground when they were infected. Given that females are substantially larger than males in natural populations, we think this size effect is likely to result in sex-biased parasite-induced vulnerability to predation (Stephenson et al 2016, Ecology and Evolution).

Infected fish (dark points) moved less distance during the escape response than uninfected fish (light points), but the effect is greatest among small fish. Here the big points give the means±SE of two size classes, split at the median (denoted by the dashed line).

Indirect effects of predators on host-parasite interactions

Thinking about host-parasite systems in isolation ignores the fact that the host and the parasite are part of a community; as such, their interactions with other species are likely to affect the way they interact with each other. One obvious example is the impact of predators on their prey as parasite hosts. Do adaptations that prey species make to predation pressure change their interaction with parasites?

I used a large-scale, long-running study of parasite distribution in natural guppy populations to address this question. Below I’ve given the main results of two papers using these data.

  • Predator-driven evolutionary change in shoaling behaviour explains the higher prevalence of directly transmitted Gyrodactylus parasites in natural guppy populations that experience high levels of predation. Guppies also show sex-biased shoaling behaviour: females shoal more in high-predation populations, but males live more solitary lives. The sex difference in infection predicted by this sex difference in behaviour is also borne out by the data (Stephenson et al 2015, Ecology).
Where there are lots of predators, female guppies (white bars) shoal more, so the parasite can transmit between them more frequently. Where there are few predators, both male (black bars) and female guppies live relatively solitary, dispersed lives. This means the parasite can transmit less frequently, and that there’s less of a sex difference in transmission. Juveniles (grey bars) experience predation from adults across all populations, so they shoal everywhere – that’s why there’s no difference in prevalence across populations among juveniles.
  • Guppies from populations that experience these high levels of predation pressure generally have much shorter life histories (i.e. they mature faster, reproduce at a younger age etc.) than those from populations that experience low levels of predation pressure. We know from other systems and theory that organisms with longer life histories should invest more in defence against parasites because their bodies have to last longer. Correspondingly, we found that among guppies from populations experiencing low levels of predation pressure, infection with Gyrodactylus was not associated with decrease in body condition, whereas in high predation populations it was. As predicted, this suggests that low predation guppies invest more in defence against parasites. (Stephenson et al 2015, Biology Letters).

In populations of guppies that experience high levels of predation (lower course), being infected with Gyrodactylus is associated with a lower body condition (scaled mass index), but in populations that experience low levels of predation (upper course) it isn’t.